Spiders were recently shown to be adversely affected by field-realistic concentrations of a broad scale of neonicotinoid insecticides. Among the reported effects of neonicotinoids on invertebrates were declines in lipid biosynthesis and upregulation of β-oxidation, while vertebrate models suggest increased adipogenesis following treatment with neonicotinoids. Therefore, we hypothesized that there exists synergy between the effects of diet and concurrent exposure to field-realistic concentrations of neonicotinoid insecticides. To address this hypothesis, we fed first instars of the large wolf spider Hogna antelucana with two types of diets and exposed them to field-realistic concentrations of three formulations of neonicotinoids (thiamethoxam, thiacloprid and acetamiprid). We then measured the growth of the tested spiders; the lipid and protein content of their bodies; and their behavior, including ballooning, rappelling, and locomotor parameters. The two tested diets consisted of casein-treated and sucrose-treated Drosophila melanogaster. The dietary treatments affected the lipid and protein content of the spiders, their body weight and carapace length but did not affect any of the measured behavioral parameters. Surprisingly, we did not find any effects of acute exposure to neonicotinoid insecticides on the lipid or protein reserves of spiders. Exposure to neonicotinoids altered the behavior of the spiders as reported previously in other spider species; however, these effects were not affected by dietary treatments. Overall, the dietary treatments did not have any major synergy with acute exposure to field-realistic concentrations of neonicotinoid insecticides.

3rd Faculty of Medicine Charles University Ruská 87 100 00 Prague Czech Republic

Crop Research Institute Prague Czech Republic

Department of Integrative Biology Oklahoma State University Stillwater OK USA

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Holmstrum P, et al. Interactions between effects of environmental chemicals and natural stressors: A review. Sci. Total Environ. 2010;408:3746–3762. doi: 10.1016/j.scitotenv.2009.10.067. PubMed DOI

Wahl O, Ulm K. Influence of pollen feeding and physiological condition on pesticide sensitivity of the honey bee Apis mellifera carnica. Oecologia. 1983;59:106–128. doi: 10.1007/BF00388082. PubMed DOI

Schmehl DR, Teal PEA, Frazier JL, Grozinger CM. Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera) J. Insect Physiol. 2014;71:177–190. doi: 10.1016/j.jinsphys.2014.10.002. PubMed DOI

Tosi S, Nieh JC, Sgolastra F, Cabbri R, Medrzycki P. Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees. Proc. Biol. Sci. 2017;284:20171711. PubMed PMC

Stuligross C, Williams NM. Pesticide and resource stressors additively impair wild bee reproduction. Proc. Biol. Sci. 2020;287:20201390. PubMed PMC

Liess M, Foit K, Knillmann S, Schäfer RB, Liess H-D. Predicting the synergy of multiple stress effects. Sci. Rep. 2016;6:32965. doi: 10.1038/srep32965. PubMed DOI PMC

Goulson D, Nicholls E, Botias C, Rotheray EL. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. 2015;347:1255957. doi: 10.1126/science.1255957. PubMed DOI

Simpson SJ, Raubenheimer D. The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity. Princeton University Press; 2012.

Simpson SJ, Le Couteur DG, Raubenheimer D. Putting the balance back in diet. Cell. 2015;161:18–23. doi: 10.1016/j.cell.2015.02.033. PubMed DOI

Wise D. Food limitation of the spider Linyphia marginata: Experimental field studies. Ecology. 1975;56:637–646. doi: 10.2307/1935497. DOI

Bilde T, Toft S. Quantifying food limitation of arthropod predators in the field. Oecologia. 1998;115:54–58. doi: 10.1007/s004420050490. PubMed DOI

Wilder SM, Rypstra A. Diet quality affects mating behaviour and egg production in a wolf spider. Anim. Behav. 2008;76:439–445. doi: 10.1016/j.anbehav.2008.01.023. DOI

Tanaka K, Itô Y. Decrease in respiratory rate in a wolf spider, Pardosa astrigera (L. Koch), under starvation. Res. Popul. Ecol. 1982;24:360–374. doi: 10.1007/BF02515582. DOI

O'Connor KI, Taylor AC, Metcalfe NB. The stability of standard metabolic rate during a period of food deprivation in juvenile Atlantic salmon. J. Fish Biol. 2000;57:41–51. doi: 10.1111/j.1095-8649.2000.tb00774.x. DOI

McCue MD. Specific dynamic action: A century of investigation. Comp. Biochem. Physiol. A. 2006;144:381394. doi: 10.1016/j.cbpa.2006.03.011. PubMed DOI

Secor SM. Specific dynamic action: A review of the postprandial metabolic response. J. Comp. Physiol. B. 2009;179:1–56. doi: 10.1007/s00360-008-0283-7. PubMed DOI

Van Leeuwen TE, Rosenfeld JS, Richards JG. Effects of food ration on SMR: Influence of food consumption on individual variation in metabolic rate in juvenile coho salmon (Onchorhynchus kisutch) J. Anim. Ecol. 2012;81:395–402. doi: 10.1111/j.1365-2656.2011.01924.x. PubMed DOI

Parthasarathy B, Somanathan H. Body condition and food shapes group dispersal but not solitary dispersal in a social spider. Behav. Ecol. 2018;29:619–627. doi: 10.1093/beheco/ary013. DOI

Koemel NA, Barnes CL, Wilder SM. Metabolic and behavioral responses of predators to prey nutrient content. J. Insect Physiol. 2019;116:25–31. doi: 10.1016/j.jinsphys.2019.04.006. PubMed DOI

Řezáč M, Řezáčová V, Heneberg P. Neonicotinoid insecticides limit the potential of spiders to re-colonize disturbed agroecosystems when using silk-mediated dispersal. Sci. Rep. 2019;9:12272. doi: 10.1038/s41598-019-48729-6. PubMed DOI PMC

Řezáč M, Řezáčová V, Heneberg P. Contact application of neonicotinoids suppresses the predation rate in different densities of prey and induces paralysis of common farmland spiders. Sci. Rep. 2019;9:5724. doi: 10.1038/s41598-019-42258-y. PubMed DOI PMC

Fagan WF, et al. Nitrogen in insects: implications for trophic complexity and species diversification. Am. Nat. 2002;160:784–802. doi: 10.1086/343879. PubMed DOI

Raubenheimer D, Mayntz D, Simpson SJ, Tøft S. Nutrient-specific compensation following diapause in a predator: Implications for intraguild predation. Ecology. 2007;88:2598–2608. doi: 10.1890/07-0012.1. PubMed DOI

Lease HM, Wolf BO. Exoskeletal chitin scales iso¬metrically with body size in terrestrial insects. J. Morphol. 2010;271:759–768. PubMed

Wilder SM, Norris M, Lee RW, Raubenheimer D, Simpson SJ. Arthropod food webs become increasingly lipid-limited at higher trophic levels. Ecol. Lett. 2013;16:895–902. doi: 10.1111/ele.12116. PubMed DOI

Salomon M, Mayntz D, Lubin Y. Colony nutrition skews reproduction in a social spider. Behav. Ecol. 2008;19:605–611. doi: 10.1093/beheco/arn008. DOI

Jensen K, Mayntz D, Wang T, Simpson SJ, Overgaard J. Metabolic consequences of feeding and fasting on nutritionally different diets in the wolf spider Pardosa prativaga. J. Insect Physiol. 2010;56:1095–1100. doi: 10.1016/j.jinsphys.2010.03.001. PubMed DOI

Jensen K, Mayntz D, Toft S, Raubenheimer D, Simpson SJ. Nutrient regulation in a predator, the wolf spider Pardosa prativaga. Anim. Behav. 2011;81:993–999. doi: 10.1016/j.anbehav.2011.01.035. DOI

Wiggins WD, Wilder SM. Mismatch between dietary requirements for lipid by a predator and availability of lipid in prey. Oikos. 2018;127:1024–1032. doi: 10.1111/oik.04766. DOI

Uetz GW, Bischoff J, Raver J. Survivorship of wolf spiders (Lycosidae) reared on different diets. J. Arachnol. 1992;20:207–211.

Sigsgaard L, Toft S, Villareal S. Diet-dependent survival, development and fecundity of the spider Atypena formosana (Oi) (Araneae: Linyphiidae) implications for biological control in rice. Biocontrol Sci. Technol. 2001;11:233–244. doi: 10.1080/09583150120035657. DOI

Fisker EN, Toft S. Effects of chronic exposure to a toxic prey in a generalist predator. Physiol. Entomol. 2004;29:129–138. doi: 10.1111/j.1365-3032.2004.00376.x. DOI

Jensen K, Mayntz D, Toft S, Raubenheimer D, Simpson SJ. Prey nutrient composition has different effects on Pardosa wolf spiders with dissimilar life histories. Oecologia. 2011;165:577–583. doi: 10.1007/s00442-010-1811-1. PubMed DOI

Wilder SM. Spider nutrition: An integrative perspective. Adv. Insect Physiol. 2011;40:87–136. doi: 10.1016/B978-0-12-387668-3.00002-7. DOI

Barnes CL, Hawlena D, Wilder SM. Predators buffer the effects of variation in prey nutrient content for nutrient deposition. Oikos. 2019;128:360–367. doi: 10.1111/oik.05685. DOI

Jensen K, et al. Optimal foraging for specific nutrients in predatory beetles. Proc. R. Soc. B. 2012;279:2212–2218. doi: 10.1098/rspb.2011.2410. PubMed DOI PMC

Toft S, Macías-Hernández N. Metabolic adaptations for isopod specialization in three species of Dysdera spiders from the Canary Islands. Physiol. Entomol. 2017;42:191–198. doi: 10.1111/phen.12192. DOI

Barry KL, Wilder SM. Macronutrient intake affects reproduction of a predatory insect. Oikos. 2013;122:1058–1064. doi: 10.1111/j.1600-0706.2012.00164.x. DOI

Wilder SM, Schneider JM. Micronutrient consumption by female Argiope bruennichi affects offspring survival. J. Insect Physiol. 2017;100:128–132. doi: 10.1016/j.jinsphys.2017.06.007. PubMed DOI

Demaree SR, Gilbert CD, Mersmann HJ, Smith SB. Conjugated linoleic acid differentially modifies fatty acid composition in subcellular fractions of muscle and adipose tissue but not adiposity of postweaning pigs. J. Nutr. 2002;132:3272–3279. doi: 10.1093/jn/132.11.3272. PubMed DOI

Nagao K, Yanagita T. Conjugated fatty acids in food and their health benefits. J. Biosci. Bioeng. 2005;100:152–157. doi: 10.1263/jbb.100.152. PubMed DOI

Hennessy AA, Ross PR, Fitzgerald GF, Stanton C. Sources and bioactive properties of conjugated dietary fatty acids. Lipids. 2016;51:377–397. doi: 10.1007/s11745-016-4135-z. PubMed DOI

Hawley J, Simpson SJ, Wilder SM. Effects of prey macronutrient content on body composition and nutrient intake in a web-building spider. PLoS ONE. 2014;9:e99165. doi: 10.1371/journal.pone.0099165. PubMed DOI PMC

Whitehorn PR, O’Connor S, Wackers FL, Goulson D. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science. 2012;336:351–352. doi: 10.1126/science.1215025. PubMed DOI

Dicks L. Bees, lies and evidence-based policy. Nature. 2013;494:283. doi: 10.1038/494283a. PubMed DOI

Rundlöf M, et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature. 2015;521:77–80. doi: 10.1038/nature14420. PubMed DOI

Tsvetkov N, et al. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science. 2017;356:1395–1397. doi: 10.1126/science.aam7470. PubMed DOI

Woodcock BA, et al. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science. 2017;356:1393–1395. doi: 10.1126/science.aaa1190. PubMed DOI

Song F, et al. Specific loops D, E and F of nicotinic acetylcholine receptor β1 subunit may confer imidacloprid selectivity between Myzus persicae and its predatory enemy Pardosa pseudoannulata. Insect Biochem. Mol. Biol. 2009;39:833–841. doi: 10.1016/j.ibmb.2009.09.009. PubMed DOI

Korenko S, Sýkora J, Řezáč M, Heneberg P. Neonicotinoids suppress contact chemoreception in a common farmland spider. Sci. Rep. 2020;10:7019. doi: 10.1038/s41598-020-63955-z. PubMed DOI PMC

Benamú M, et al. Nanostructural and mechanical property changes to spider silk as a consequence of insecticide exposure. Chemosphere. 2017;181:241–249. doi: 10.1016/j.chemosphere.2017.04.079. PubMed DOI

Korenko S, Saska P, Kysilková K, Řezáč M, Heneberg P. Prey contaminated with neonicotinoids induces feeding deterrent behavior of a common farmland spider. Sci. Rep. 2019;9:15895. doi: 10.1038/s41598-019-52302-6. PubMed DOI PMC

Park Y, et al. Imidacloprid, a neonicotinoid insecticide, potentiates adipogenesis in 3T3-L1 adipocytes. J. Agric. Food Chem. 2013;61:255–259. doi: 10.1021/jf3039814. PubMed DOI

Sun Q, et al. Imidacloprid promotes high fat diet-induced adiposity in female C57BL/6J mice and enhances adipogenesis in 3T3-L1 adipocytes via the AMPKα-mediated pathway. J. Agric. Food Chem. 2017;65:6572–6581. doi: 10.1021/acs.jafc.7b02584. PubMed DOI PMC

Sun Q, et al. Imidacloprid promotes high fat diet-induced adiposity and insulin resistance in male C57BL/6J mice. J. Agric. Food Chem. 2016;64:9293–9306. doi: 10.1021/acs.jafc.6b04322. PubMed DOI PMC

McCluney KE, Sabo JL. Water availability directly determines per capita consumption at two trophic levels. Ecology. 2009;90:1463–1469. doi: 10.1890/08-1626.1. PubMed DOI

McCluney KE, Sabo JL. Tracing water sources of terrestrial animal populations with stable isotopes: Laboratory tests with crickets and spiders. PLoS ONE. 2010;5:e15696. doi: 10.1371/journal.pone.0015696. PubMed DOI PMC

Leinbach IL, McCluney KE, Sabo JL. Predator water balance alters intraguild predation in a streamside food web. Ecology. 2019;100:e02635. doi: 10.1002/ecy.2635. PubMed DOI

Noldus LP, Spink AJ, Tegelenbosch RA. EthoVision: A versatile video tracking system for automation of behavioral experiments. Behav. Res. Methods Instrum. Comput. 2001;33:398–414. doi: 10.3758/BF03195394. PubMed DOI

Pétillon JJ, Deruytter D, Decae A, Renault D, Bonte D. Habitat use, but not dispersal limitations, as the mechanism behind the aggregated population structure of the mygalomorph species Atypus affinis. Anim. Biol. 2012;62:181–192. doi: 10.1163/157075611X617094. DOI

Radwan MA, Mohamed MS. Imidacloprid induced alterations in enzyme activities and energy reserves of the land snail, Helix aspersa. Ecotoxicol. Environ. Saf. 2013;95:91–97. doi: 10.1016/j.ecoenv.2013.05.019. PubMed DOI

Ribeiro S, Sousa JP, Nogueira AJA, Soares AMVM. Effect of endosulfan and parathion on energy reserves and physiological parameters of the terrestrial isopod Porcellio dilatatus. Ecotoxicol. Environ. Saf. 2001;49:131–138. doi: 10.1006/eesa.2001.2045. PubMed DOI

Rambabu PJ, Rao MB. Effect of an organochlorine and three organophosphate pesticides on glucose, glycogen, lipid and protein contents in tissues of the freshwater snail, Bellamya dissimilis (Müller) Bull. Environ. Contam. Toxicol. 1994;53:142–148. PubMed

Dutra BK, Fernandes FA, Lauffer AL, Oliveira GT. Carbofuran-induced alterations in the energy metabolism and reproductive behaviors of Hyalella castroi (Crustacea, Amphipoda) Comp. Biochem. Physiol. Part C. 2009;149:640–646. PubMed

Messiad R, Habes D, Soltani N. Reproductive effects of a neonicotinoid insecticide (Imidacloprid) in the German Cockroaches Blattella germanica L. (Dictyoptera, Blattellidae) J. Entomol. Zool. Stud. 2015;3:1–6.

Abdelsalam SA, Alzahrani AM, Elmenshawy OM, Sedky A, Abdel-Moneim AM. Biochemical and ultrastructural changes in the ovaries of red palm weevil, Rhynchophorus ferrugineus (Coleoptera: Curculionidae) following acute imidacloprid poisoning. J. Asia Pac. Entomol. 2020;23:709–714. doi: 10.1016/j.aspen.2020.05.010. DOI

Tufi S, Stel JM, De Boer J, Lamoree MH, Leonards PEG. Metabolomics to explore imidacloprid-induced toxicity in the central nervous system of the freshwater snail Lymnaea stagnalis. Environ. Sci. Technol. 2015;49:14529–14536. doi: 10.1021/acs.est.5b03282. PubMed DOI

Ewere EE, Reichelt-Brushett A, Benkerndorff K. Imidacloprid and formulated product impacts the fatty acids and enzymatic activities in tissues of Sydney rock oysters, Saccostrea glomerata. Mar. Environ. Res. 2019;151:104765. doi: 10.1016/j.marenvres.2019.104765. PubMed DOI

Capowiez Y, Rault M, Mazzia C, Belzunces L. Earthworm behavior as a biomarker: A case study using imidacloprid. Pedobiologia. 2003;47:542–547.

Drobne D, et al. Toxicity of imidacloprid to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea) Chemosphere. 2008;71:1326–1334. doi: 10.1016/j.chemosphere.2007.11.042. PubMed DOI

Contact exposure to neonicotinoid insecticides temporarily suppresses the locomotor activity of Pardosa lugubris agrobiont wolf spiders